REVIEW Open Access Dogs, cats, parasites, and …...of secondary bacterial infections. Some...

Dantas-Torres and Otranto Parasites & Vectors 2014, 7:22http://www.parasitesandvectors.com/content/7/1/22

REVIEW Open Access

Dogs, cats, parasites, and humans in Brazil:opening the black boxFilipe Dantas-Torres1,2* and Domenico Otranto2

Portuguese version: Please see Additional file 1 (http://www.biomedcentral.com/content/supplementary/1756-3305-7-22-S1.pdf)for the Portuguese version of this review article.

Abstract

Dogs and cats in Brazil serve as primary hosts for a considerable number of parasites, which may affect their healthand wellbeing. These may include endoparasites (e.g., protozoa, cestodes, trematodes, and nematodes) andectoparasites (i.e., fleas, lice, mites, and ticks). While some dog and cat parasites are highly host-specific (e.g., Aeluros-trongylus abstrusus and Felicola subrostratus for cats, and Angiostrongylus vasorum and Trichodectes canis for dogs),others may easily switch to other hosts, including humans. In fact, several dog and cat parasites (e.g., Toxoplasmagondii, Dipylidium caninum, Ancylostoma caninum, Strongyloides stercoralis, and Toxocara canis) are important notonly from a veterinary perspective but also from a medical standpoint. In addition, some of them (e.g., Lynxacarusradovskyi on cats and Rangelia vitalii in dogs) are little known to most veterinary practitioners working in Brazil. Thisarticle is a compendium on dog and cat parasites in Brazil and a call for a One Health approach towards a bettermanagement of some of these parasites, which may potentially affect humans. Practical aspects related to thediagnosis, treatment, and control of parasitic diseases of dogs and cats in Brazil are discussed.

Keywords: Dogs, Cats, Humans, Zoonosis, Control, South America

IntroductionThe word “parasite” (from Ancient Greek, parasitos:para = beside, sitos = food) means literally a person thateats at the table of another. In the figurative sense, cor-rupt politicians that make the use their political powerand public resources for their own benefit may be calledparasites of society. But in parasitology, a parasite is anorganism that takes benefit from another (the host),without giving something back and usually causing somedamage to it. Incidentally, parasites constitute a diversegroup of organisms that may affect a wide range of animalhosts, including amphibians, birds, fishes, mammals, andreptiles. They may be generally subdivided as endopara-sites (=internal) and ectoparasites (=external), accord-ing to their location in the host. Ectoparasites may alsobe classified as permanent (e.g., lice and mites) or non-permanent (e.g., ticks and mosquitoes), depending on the

* Correspondence: [email protected] of Immunology, Aggeu Magalhães Research Centre, OswaldoCruz Foundation, Recife Pernambuco 50670420, Brazil2Department of Veterinary Medicine, University of Bari, Valenzano 70010,Bari, Italy

© 2014 Dantas-Torres and Otranto; licensee Bthe Creative Commons Attribution License (htdistribution, and reproduction in any mediumDomain Dedication waiver (http://creativecomarticle, unless otherwise stated.

relationship with their host; i.e., whether their life cycletakes place solely on their hosts or also in the environment.Dogs and cats are the most popular pet animals world-

wide. Nowadays, dogs for example have assumed manyfunctions as guides for blind people, as therapeutic agents,as guard and hunting dogs. Moreover, in many developingcountries, both dogs and cats have become part of humanfamilies, regardless of the social class (Figure 1). The bene-fits of having a pet animal are undisputed [1], but bothdogs and cats may harbour many parasites potentiallytransmissible to humans, which may represent a healthrisk, especially to children, the elderly and the immuno-compromised [2]. For instance,Toxoplasma gondii, Dipyli-dium caninum, Echinococcus granulosus, Ancylostomabraziliense, Toxocara canis, Onchocerca lupi, and Thelaziacallipaeda are common parasites of dogs and cats thatcan affect humans in different countries around the world.This fact emphasizes the need for a One Health approachtowards a more efficient management and control of theseparasites [3,4].At the beginning of the 21st century, parasitic diseases

are still causing a severe burden on animal and human

ioMed Central Ltd. This is an Open Access article distributed under the terms oftp://creativecommons.org/licenses/by/2.0), which permits unrestricted use,, provided the original work is properly cited. The Creative Commons Publicmons.org/publicdomain/zero/1.0/) applies to the data made available in this

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Figure 1 Human-animal bond. A homeless with his inseparablefriends that were found abandoned in the streets of Porto Alegre,southern Brazil.

Figure 2 Poor living conditions. An owner and his dogs living in apoor rural community in Goiana, north-eastern Brazil, where visceralleishmaniosis is endemic. In poor rural communities people (as thisman in the picture) are used to walking barefoot, which is a riskfactor for bare feet-related diseases, such as cutaneous larva migransand tungiasis.

Dantas-Torres and Otranto Parasites & Vectors 2014, 7:22 of 25http://www.parasitesandvectors.com/content/7/1/22

populations in tropical and subtropical regions aroundthe world [5-7]. Furthermore, the impact of some ofthese diseases is disproportionally higher in developingcountries such as Brazil, because the living conditions ofthe populations often favour the exposure to certainparasites, whose transmission may be associated withpoor housing and sanitary conditions (Figure 2), as wellas with inequities in the access to education and primaryhealthcare services.Brazil is a country with continental dimensions (i.e.,

8,515,767 km2), occupying most of the land area of SouthAmerica and representing the largest economy in the re-gion. Despite the persistent social and economic inequal-ities (e.g., unequal access to education, health care andsanitation, safe drinking water and decent housing), whichhave become the dark side of the Brazilian history, the im-portance of dogs and cats as pets, as well as the demandfor high standard veterinary services, has increased overthe last decades in Brazil. Impressively, according to theAssociação Brasileira da Indústria de Produtos paraAnimais de Estimação (Abinpet), Brazil currently holdsthe world’s second largest dog and cat populations, withover 37 million dogs and 21 million cats (http://abinpet.

org.br/imprensa/mercado-pet-deve-faturar-r-154-bilhoes-em-2013). Apropos, the growing number of dogs and catsin urban areas in Brazil has been accompanied by substan-tial increases in the animal feed and pet care markets.According to Abinpet, the Brazilian pet market will earn15.4 billion Brazilian real (approximately 7 billion US dol-lars) in 2013, with an overall increase of 8.3% in compari-son with 2012. Specifically, it has been estimated that in2013 the pet service sector (services related to animal care,including bath and hair cut) will increase in 24.5%, petfood (animal feed) in 4.9%, pet care (equipments, accessor-ies and products for animal hygiene and care) in 5.2%, andpet vet (medicines) in 6.7%. These numbers pose Brazil asthe world’s second largest pet market, behind only theUnited States.The diversity of natural environments present in Brazil

is outstanding, as is its biodiversity. By the bye, dogs andcats living in Brazil may harbour a long list of parasitesthat may affect their wellbeing and eventually pose a riskto the health of their owners [8,9]. Information on theirdistribution, epidemiology, and impact on human healthis fragmentary and mainly published in Brazilian journals.In this sense, this article is a compendium on dog and catparasites in Brazil and a call for a One Health approach to-wards a better management of some of these parasites,which may potentially affect humans. Practical aspects re-lated to the diagnosis, treatment, and control of parasiticdiseases of dogs and cats in Brazil are discussed.

ReviewEctoparasites of dogs and cats in BrazilEctoparasites may cause irritation, blood depletion, prur-itus, and skin lesions, potentially leading to the occurrence

http://abinpet.org.br/imprensa/mercado-pet-deve-faturar-r-154-bilhoes-em-2013




of secondary bacterial infections. Some ectoparasites suchas fleas, lice and ticks may also transmit pathogens to dogsand cats, including bacteria, protozoa, and helminthsreviewed in Ref. [9]. Furthermore, ticks can also causetoxicosis, as it has recently been reported in a dogbitten by the mouro tick Ornithodoros brasiliensis inBrazil [10].In Brazil, dogs and cats may serve as hosts for a large

number of ectoparasites, including fleas, lice, mites, andticks (Tables 1 and 2). Indeed, dogs may be frequentlyinfested by species of fleas (e.g., Ctenocephalides canis,Ctenocephalides felis felis, and Tunga penetrans), lice(e.g., Heterodoxus spiniger and Trichodectes canis), mites

Table 1 Ectoparasites of dogs in Brazil

Phylum Class Order

Arthropoda Arachnida Ixodida

Sarcoptiformes

Trombidiformes

Insecta Phthiraptera

Siphonaptera

aChecklist of ectoparasites (flying insects excluded) infesting dogs in Brazil [11-41].

(e.g., Demodex canis, Otodectes cynotis, and Sarcoptes scabiei)and ticks (e.g., Amblyomma aureolatum, Amblyomma ovale,and Rhipicephalus sanguineus sensu lato) [11-41]. Whilesome flea species may be common in rural settings (e.g.,T. penetrans), C. felis felis is indeed the most common fleainfesting dogs in Brazil. Other less common ectoparasites(e.g., the flea Rhopalopsyllus lutzi lutzi) have also been re-ported in dogs in Brazil [21,28]. In a similar manner, thefindings of some wildlife-associated ticks (e.g., Amblyommalongirostre, Amblyomma naponsense, Amblyomma nodosum,Amblyomma pacae, Amblyomma scalpturatum, andHaemaphysalis juxtakochi) on dogs in Brazil are inci-dental findings and of unknown clinical significance.

Family Speciesa

Argasidae Ornithodoros brasiliensis

Ornithodoros rostratus

Ixodidae Amblyomma aureolatum

Amblyomma cajennense

Amblyomma longirostre

Amblyomma naponsense

Amblyomma nodosum

Amblyomma oblongoguttatum

Amblyomma ovale

Amblyomma pacae

Amblyomma parvum

Amblyomma scalpturatum

Amblyomma tigrinum

Haemaphysalis juxtakochi

Rhipicephalus microplus

Rhipicephalus sanguineus s.l.

Psoroptidae Otodectes cynotis

Sarcoptidae Notoedres cati

Sarcoptes scabiei

Demodicidae Demodex canis

Boopidae Heterodoxus spiniger

Linognathidae Linognathus setosus

Trichodectidae Trichodectes canis

Ceratophyllidae Nosopsyllus fasciatus

Tungidae Tunga penetrans

Pulicidae Ctenocephalides canis

Ctenocephalides felis felis

Pulex irritans

Xenopsylla brasiliensis

Xenopsylla cheopis

Rhopalopsyllidae Rhopalopsyllus lutzi lutzi

Table 2 Ectoparasites of cats in Brazil

Phylum Class Order Family Speciesa

Arthropoda Arachnida Ixodida Ixodidae Amblyomma aureolatum

Amblyomma ovale

Amblyomma triste

Rhipicephalus sanguineus s.l.

Sarcoptiformes Listrophoridae Lynxacarus radovskyi

Psoroptidae Otodectes cynotis

Sarcoptidae Notoedres cati

Sarcoptes scabiei

Trombidiformes Demodicidae Demodex cati

Insecta Phthiraptera Trichodectidae Felicola subrostratus

Siphonaptera Pulicidae Ctenocephalides canis


Pulex irritans

Tungidae Tunga penetransaChecklist of ectoparasites (flying insects excluded) infesting cats in Brazil [19,22,42-49].


Cats in Brazil are frequently found infested by fleas (e.g.,C. canis, C. felis felis, P. irritans, and T. penetrans), lice(Felicola subrostratus), and mites (e.g., D. cati, Lynxacarusradovskyi, Notoedres cati, and O. cynotis) [19,22,42-49].Less frequently, they have been found infested by tickssuch as R. sanguineus s.l. and Amblyomma triste [49,50].Some of these ectoparasites are well known in certain re-gions (e.g., L. radovskyi in north-eastern Brazil), but com-pletely unknown or considered rare in others. Even if catshave more knowhow than dogs when the issue is “ectopara-site removal” by grooming, they may be highly exposed toectoparasites, particularly in high-density situations such asin catteries [45].Even if most fleas, lice, mites, and ticks infesting dogs

and cats may be easily identified, the delineation of somespecies may be troublesome for non-taxonomists[51,52]. While some keys for fleas, lice, and ticks havebeen published in books [13,14,53] and journals [54-56],there are no comprehensive pictorial keys for the identi-fication of dog and cat ectoparasites in Brazil (see Table 3and Figure 3).Flying insects may also represent a significant clinical

problem to dogs as cats in Brazil [9,57-66]. For instance,mosquitoes, phlebotomine sand flies and triatomine bugsare vectors of Dirofilaria immitis, Leishmania infantum,and Trypanosoma cruzi, respectively, to both dogs andcats [9]. Myiasis is also quite a common problem in dogsand cats in Brazil, being most frequently associated withinfestation by larvae of Cochliomyia hominivorax andDermatobia hominis [58-65], and less commonly by otherspecies of flies (e.g., Lucilia eximia) [57,65]. Furthermore,stable flies (Stomoxys calcitrans) can produce skin lesionson the ears of these animals, which may also lead to theoccurrence of secondary bacterial infections [9,66].

Endoparasites of dogs and cats in BrazilIn addition to ectoparasites, dogs in Brazil may be affectedby numerous endoparasites (Table 4), including protozoa,cestodes (tapeworms), trematodes (flukes), and nematodes(roundworms) [32,67-130]. For instance, endoparasitessuch as Dipylidium caninum, Echinococcus granulosus, A.braziliense, Ancylostoma caninum, Strongyloides stercoralis,Toxocara canis, Trichuris vulpis, and Dirofilaria immitisare commonly found in dogs from different Brazilian re-gions [67,69]. Other endoparasites such as Angiostrongylusvasorum have only sporadically been reported in Brazil[74]. Similarly, cats have frequently been found affectedby several endoparasites (Table 5) in Brazil, includingT. gondii, D. caninum, Taenia taeniformis, Spirometramansonoides, Aelurostrongylus abstrusus, A. braziliense,A. caninum, A. tubaeforme, Toxascaris leonina, Toxo-cara cati, Pearsonema feliscati, Trichuris campanula,Trichuris serrata, Physaloptera praeputialis, and Platy-nosomum fastosum [47,71,87,90,92,97,131-137]. Less com-mon endoparasites have also been reported in cats, such asthe acanthocephalan Sphaerirostris erraticus [137].Dogs have been found infected by vector-borne proto-

zoa, including Babesia gibsoni, Babesia vogeli, Rangeliavitalii, Hepatozoon canis, Leishmania amazonensis, Leish-mania braziliensis, Leishmania infantum, Trypanosomacruzi, and Trypanosoma evansi [73,78-82,85,87-90,96,102-104,109-113,117-121,124,128-130]. Other protozoa of un-known pathogenicity (e.g., Trypanosoma caninum) havealso been described in Brazilian dogs [108]. In addition,other vector-borne organisms have also been frequentlyreported in dogs, including Anaplasma platys, Ehrlichiacanis and, less frequently, Rickettsia rickettsii [9].Cats have also been found infected by vector-borne

protozoa such as B. vogeli, Cytauxzoon felis, H. canis,

Table 3 Key for ectoparasites identification

1a Three pairs of legs 2

1b Four pairs of legs 13

2a Body laterally flattened (SIPHONAPTERA) 3

2b Body dorsoventrally flattened (PHTHIRAPTERA) 10

3a Pronotal and/or genal ctenidia present 4

3b Pronotal and genal ctenidia absent 6

4a Genal ctenidium absent and pronotal ctenidium present Nosopsyllus fasciatus

4b Genal and pronotal ctenidia present 5

5a Genal ctenidium with the first seta much shorter than the others (Figure 3A; arrowhead); posterior tibia with twosimple setae between the penultimate and the last double setae (Figure 3A; arrows)

Ctenocephalides canis

5b Genal ctenidium with the first seta approximately the same length of the remaining (Figure 3B; arrowhead);posterior tibia with one simple seta between the penultimate and the last double setae (Figure 3B; arrow)


6a Thoracic segments narrow (Figure 3C; arrow), ocular and occipital setae absent; front of the head angular(upturned) (Figure 3C; arrowhead)

Tunga penetrans

6b Not as above 7

7a Abdominal segments with two rows of setae in the dorsal border Rhopalopsyllus lutzi lutzi

7b Abdominal segments with one row of setae in the dorsal border 8

8a Occipital region with one seta (Figure 3D; arrow) Pulex irritans

8b Occipital region with two rows of setae arranged in a “V” 9

9a Male antepygidial seta inserted on a discrete tubercle; female with body of spermatheca (in black) not larger thanthe base of tail (Figure 3E)

Xenopsylla cheopis

9b Male antepygidial seta inserted on a well-developed tubercle; female with body of spermatheca (in black) largerthan the base of tail (Figure 3F)

Xenopsylla brasiliensis

10a Head longer than large (Figure 3G; arrow); sucking mouthparts Linognathus setosus

10b Head as large as long; chewing mouthparts 11

11a Tarsus with two claws (Figure 3H; arrow) Heterodoxus spiniger

11b Tarsus with one claw 12

12a Head rounded anteriorly (Figure 3I) Trichodectes canis

12b Head triangular in shape (Figure 3J) Felicola subrostratus

13a Body length equal or less than 0.5 mm; Haller’s organ absent 14

13b Body length larger than 0.5 mm; Haller’s organ present on first tarsi (IXODIDA) 19

14a Body carrot-shaped or with a bell pepper shape (TROMBIDIFORMES) 15

14b Body not as above, usually rounded in shape (SARCOPTIFORMES) 16

15a Body long and slender (carrot-shaped) (Figure 3K) Demodex spp.a

15b Body with a bell pepper shape; well-developed mouthparts; palpi that end in prominent hooks (Figure 3L; arrow) Cheyletiella spp.b

16a Body rounded 17

16b Body cylindrical and elongate, heavily striated (Figure 3M) Lynxacarus radovskyi

17a Legs long, with short, unjointed pedicels (Figure 3N) Otodectes cynotis

17b Legs short, with long, unjointed pedicels 18

18a Anus dorsal (Figure 3O; arrow) Notoedres cati

18b Anus terminal (Figure 3P; arrow); body surface covered by several triangular spines arranged in rows Sarcoptes scabiei

19a Inornate; basis capituli hexagonal; coxa I bifid Rhipicephalussanguineus s.l.c

19b Usually ornate; basis capituli variable in form Amblyomma spp.d

aDemodex canis in dogs and Demodex cati in cats.bNo bona fide data on Cheyletiella spp. in dogs or cats in Brazil.cAt least two distinct biologically and genetically distinct tick populations under the name “R. sanguineus” have been found on dogs in South America [52,161,162].dSeveral species reported in dogs and cats. Amblyomma aureolatum, Amblyomma cajennense and Amblyomma ovale are among the most common Amblyommaspecies found on rural dogs in Brazil [55].


Figure 3 Ectoparasites of dogs and cats. Line drawings for the identification of common dog and cat ectoparasites (fleas: A-F; lice: G-J andmites: K-P) found in Brazil. For details see Table 3).


Hepatozoon felis, L. amazonensis, L. braziliensis, andL. infantum [42,44,129,136,138-148]. Indeed, the diver-sity of endoparasites of cats and dogs in Brazil is impres-sive, but certainly underestimated, mainly because moststudies carried out in this country have been based on thedetection and identification of eggs and oocysts in faecalsamples using ordinary coprological techniques. This em-phasizes the need for additional diagnostic methods (e.g.,coproantigen tests, molecular tests or post-mortem exam-ination) if we are to understand the actual diversity andprevalence of endoparasites of dogs and cats in Brazil.

Geographical distribution and prevalenceDog and cat parasites are widespread in Brazil and inmost cases occur virtually in all geographical regions(north, northeast, south, southeast, and centre-west) ofthe country. However, for several common external par-asites (e.g., D. canis, N. cati e O. cynotis) and internal(e.g., D. caninum, A. brasiliense e T. canis) there is rela-tively limited published information, particularly ininternational journals. Therefore, it is presently difficultto generate informative, bona fide maps for most dog

and cat parasites occurring in Brazil, even if most of theseparasites are certainly present in all regions of the country.For instance, in a study carried out in south-eastern Brazil,155 dogs were necropsied and D. caninum was diag-nose in 57 (36.8%) of them, A. caninum in 30 (19.4%),and T. canis in 24 (15.5%) [36]. Similarly, a study con-ducted in north-eastern Brazil, revealed that A. caninum(prevalence, 95.7%) was the most prevalent endoparasitein 46 stray dogs necropsied, followed by D. caninum(45.7%), T. canis (8.7%), and T. vulpis (4.3%) [32]. Thesestudies indicate high prevalence rates of infestation byendoparasites in stray dogs from different Brazilian re-gions representing a permanent source of endoparasitesto pet animals and a major zoonotic hazard for humans,through the contamination of public parks and beaches(see “Dogs, cats, parasites and humans: public healthaspects”).Stray cats are also frequently exposed to endoparasites.

For instance, a study conducted in south-eastern Brazil re-ported infestations by A. braziliense (67.3%), A. caninum(21.1%), and A. tubaeforme (9.6%) in 52 cats necropsied[116]. Similarly, in a recent study conducted in centre-

Table 4 Endoparasites of dogs in Brazil


Apicomplexa Aconoidasida Piroplasmida Babesiidae Babesia gibsoni

Babesia vogeli

Theileriidaeb Rangelia vitalii

Conoidasida Eucoccidiorida Hepatozoidae Hepatozoon canis

Cryptosporidiidae Cryptosporidium canis

Eimeridae Isospora canis (syn. Cystoisospora canis)

Isospora ohioensis (syn. Cystoisospora ohioensis)

Sarcocystidae Hammondia heydorni

Neospora caninum

Sarcocystis capracanis

Sarcocystis cruzi (syn. Sarcocystis bovicanis)

Sarcocystis levinei

Sarcocystis miescheriana (syn. Sarcocystis suicanis)

Sarcocystis tenella (syn. Sarcocystis ovicanis)

Metamonada Parabasalia Trichomonadida Trichomonadidae Pentatrichomonas hominis (syn. Trichomonas hominis)

Sarcomastigophora Zoomastigophora Diplomonadida Hexamitidae Giardia duodenalis (syn. Giardia intestinalis)

Kinetoplastida Trypanosomatidae Leishmania infantum (syn. Leishmania chagasi)

Leishmania amazonensis

Leishmania braziliensis

Trypanosoma caninum

Trypanosoma evansi

Trypanosoma cruzi

Nematoda Secernentea Strongylida Ancylostomatidae Ancylostoma braziliense

Ancylostoma caninum

Angiostrongylidae Angiostrongylus vasorum

Rhabditida Strongyloididae Strongyloides stercoralis

Ascaridida Ascarididae Lagochilascaris minor

Toxascaris leonina

Toxocara canis

Dioctophymatidae Dioctophyme renale

Trichurida Trichinellidae Calodium hepaticum (syn. Capillaria hepatica)

Trichuridae Trichuris vulpis

Spirurida Gongylonematidae Gongylonema pulchrum

Onchocercidae Acanthocheilonema reconditum

Cercopithifilaria bainae

Cercopithifilaria grassii (syn. Dipetalonema grassii)

Dirofilaria immitis

Physalopteridae Physaloptera praeputialis

Spirocercidae Spirocerca lupi


Table 4 Endoparasites of dogs in Brazil (Continued)

Platyhelminthes Cestoda Cyclophyllidea Dipylidiidae Dipylidium caninum

Taeniidae Echinococcus granulosus

Taenia hydatigena

Taenia multiceps (syn. Multiceps multiceps)

Trematoda Opisthorchiida Heterophyidae Ascocotyle longa (syn. Phagicola arnaldoi)

Acanthocephala Archiacanthocephala Oligacanthorhynchida Oligacanthorhynchidae Oncicola canisaChecklist of endoparasites (protozoa and helminths) affecting dogs in Brazil [32,67-130,344-353] Doubtful records (e.g., Phagicola minuta, Aelurostrongylusabstrusus, Dirofilaria repens, Necator americanus, Trichuris serrata, Uncinaria stenocephala, Isospora rivolta, and Isospora bigemina) [68,69] are not included.bThe genus Rangelia has long been regarded a synonym of Babesia (family Babesiidae), but recent genetic and biological data supports its validity and itsinclusion in the family Theileriidae. The creation of a monospecific family (Rangeliidae) does not seem desirable.


western Brazil, 146 cats were necropsied and 98 of themwere infested by roundworms [A. braziliense (50.68%);A. tubaeforme (10.27%); T. cati (4.11%); P. praeputialis(2.05%); P. feliscati (3.42%); and A. abstrusus (1.37%)],cestodes [S. mansonoides (4.11%); D. caninum (3.42%); andT. taeniformis (0.68%)], trematodes [P. fastosum (26.03%)],and acanthocephalans [S. erraticus (3.42%)] [137]. Again,these studies reveal a considerable diversity of endopara-sites in cats from different Brazilian regions, with relativelyhigh prevalence rates.The geographical distribution of vector-borne protozoa

and heminths of dogs has been reviewed elsewhere [9].For instance, L. infantum is widespread in all Brazilianregions [81,113,149,150], but less frequent in southernparts of the country [151,152]. However, L. longipalpis,the principal vector for L. infantum, is present in northernArgentina [153], Paraguay [154], and has recently beendetected in Uruguay [155]. Furthermore, L. longipalpisis abundant in Mato Grosso do Sul State [156], whichmakes border with Paraná State in southern Brazil. Lastbut not least, the presence of L. longipalpis in Rio Grandedo Sul (the southernmost Brazilian state) has been proven[157]. These findings may suggest that L. longipalpis mayhave already colonized other areas of southern Brazil andthat canine leishmaniosis may become a problem in thatregion in the near future.The little known protozoan R. vitalii occurs mainly in

southern and south-eastern Brazil [119,124,158,159], whereticks such as A. aureolatum, the putative vector, arecommonly found in dogs frequenting the Atlantic rain-forest environment [160]. Interestingly, B. gibsoni hasbeen reported exclusively in southern Brazil [87,104],which also suggests that R. sanguineus s.l. is not the vec-tor of this protozoan in Brazil, considering that this tickis prevalent in virtually all regions of the country[52,161,162]. In fact, pathogens that are transmitted byR. sanguineus s.l. (e.g., B. vogeli and Ehrlichia canis) areusually widespread in Brazil [9], not concentrated in aspecific region as it occurs with B. gibsoni. In any case,the possibility that R. sanguineus s.l. ticks are acting asvectors of B. gibsoni in Brazil cannot be ruled out.

Ctenocephalides spp. fleas are also widespread in Brazil[18,35,36,38,129], but C. felis felis surpasses C. canis indistribution, the latter being reputed to be more commonin regions with more temperate climates, as in the south-east and south of the country [51]. Indeed, C. felis felis hasbeen reported in 17 states (Alagoas, Amazonas, Bahia,Ceará, Espírito Santo, Goiás, Mato Grosso, Minas Gerais,Paraíba, Paraná, Pernambuco, Rio de Janeiro, Rio Grandedo Norte, Rio Grande do Sul, Roraima, Santa Catarina,and São Paulo), while C. canis has been reported in onlynine (Amazonas, Bahia, Maranhão, Minas Gerais, Paraná,Pernambuco, Rio Grande do Sul, Santa Catarina, andSão Paulo) [51]. As a consequence of the widespreaddistribution of Ctenocephalides spp. fleas on dogs andcats, flea-borne parasites like D. caninum and A. recon-ditum [163-167] are widespread in Brazil as reviewedin Ref. [9].Even if fleas, lice and ticks may be found infesting dogs

in all Brazilian regions, the distribution and prevalence atthe local level may vary widely, also according to climateconditions and the degree of urbanization of each area.For instance, in a study conducted in north-eastern Brazil,the frequency of infestation by R. sanguineus s.l. tended tobe higher in urban than in rural areas, whereas infestationsby Amblyomma ticks and C. felis felis was more commonon rural dogs [39]. In the same study, mixed infestationswere significantly more frequent on rural than on urbandogs. Nonetheless, even if R. sanguineus s.l. ticks are moreprevalent in urban settings [18,28,32], they may infest ahigh proportion of rural dogs in some areas [30,33,36].Serological surveys have also reported moderate to high

levels of exposure to parasites such as Neospora caninumand T. gondii in dogs and cats in Brazil [151,168-173]. Forinstance, in a recent study carried out in south-easternBrazil, 386 cats were assayed by indirect immunofluores-cence antibody tests (IFAT) for the presence of antibodiesagainst T. gondii and 63 (16.3%) of them were positive[172]. Prevalence rates of anti-N. caninum antibodies indogs ranging from 26% to 34.5% were reported innorth-eastern Brazil, with 57.6% of the seropositive dogsalso being positive for anti-T. gondii antibodies [169]. In

Table 5 Endoparasites of cats in Brazil


Sarcomastigophora Zoomastigophora Diplomonadida Hexamitidae Giardia duodenalis

Kinetoplastida Trypanosomatidae Leishmania infantum

Leishmania amazonensis

Leishmania braziliensis

Trypanosoma cruzi

Apicomplexa Aconoidasida Piroplasmida Babesiidae Babesia vogeli

Theileriidae Cytauxzoon felis

Conoidasida Eucoccidiorida Hepatozoidae Hepatozoon canis

Hepatozoon felis

Cryptosporidiidae Cryptosporidium felis

Eimeriidae Isospora felis (syn. Cystoisospora felis)

Isospora felis (syn. Cystoisospora rivolta)

Sarcocystidae Hammondia hammondi

Sarcocystis hirsuta (syn. Sarcocystis bovifelis)

Toxoplasma gondii

Nematoda Secernentea Strongylida Ancylostomatidae Ancylostoma braziliense

Ancylostoma caninum

Ancylostoma tubaeforme

Angiostrongylidae Aelurostrongylus abstrusus

Gurltia paralysans

Syngamidae Mammomonogamus dispar

Rhabditida Strongyloididae Strongyloides stercoralis

Ascaridida Ascarididae Lagochilascaris minor

Toxascaris leonina

Toxocara cati (syn. Toxocara mistax)

Dioctophymatidae Dioctophyme renale

Trichurida Capillariidae Calodium hepaticum (syn. Capillaria hepatica)

Pearsonema feliscati

Trichuridae Trichuris campanula

Trichuris serrata

Spirurida Onchocercidae Dirofilaria immitis

Physalopteridae Physaloptera praeputialis

Platyhelminthes Cestoda Cyclophyllidea Dipylidiidae Dipylidium caninum

Taeniidae Taenia taeniformis

Pseudophyllidea Diphyllobothriidae Spirometra mansonoides

Trematoda Opisthorchiida Heterophyidae Ascocotyle angrense

Ascocotyle longa (syn. Phagicola arnaldoi)

Plagiorchiida Dicrocoeliidae Platynosomum fastosum

Strigeatida Diplostomatidae Alaria alata

Acanthocephala Archiacanthocephala Moniliformida Moniliformidae Moniliformis moniliformis

Palaecanthocephala Polymorphida Centrorhynchidae Sphaerirostris erraticusaChecklist of endoparasites (protozoa and helminths) affecting cats in Brazil [42,44,47,71,87,90,92,97,129,131-148,346,349,352-356]. Doubtful records (e.g., Ascaridiagalli and Heterakis gallinarum) [68,69] are not included.



another study conducted in south-eastern Brazil, 703 dogsfrom urban and rural areas were tested for N. caninumand 11.4% of them were positive. The likelihood of beingpositive to N. caninum was associated with dogs aged >4years, guard dogs, hunting dogs, and with dogs from dairyfarms with a history of bovine abortion [173]. In particular,among rural dogs, an association with seroprevalence wasrecorded for milk farms, dogs not fed with commercialfood, hunting, and guard dogs. Altogether, these studiesreveal that dogs and cats from different regions bothrural and urban areas are at risk of infection by parasitessuch as N. caninum and T. gondii. This is also true forLeishmania spp. in dogs, for which seroprevalence rateshigher than 60% have been reported in some highlyendemic areas [168].

Seasonal dynamics in the tropicsInformation on the ecology of parasites of dogs andcats in Brazil is fragmentary, meagre, and, for severalparasites, completely lacking. Considering the variety ofbiomes (Atlantic Rainforest, Amazon, Pantanal, Cerrado,Caatinga, and Pampa) and climates (from tropical northto temperate zones below the Tropic of Capricorn) regis-tered in Brazil, the seasonal dynamics of dog and cat para-site populations would be expectedly variable from regionto region. Nonetheless, the climate conditions in Brazil areso suitable that a range of arthropod vectors are found theyear-round. For instance, studies carried out in an area ofD. immitis endemicity in Rio de Janeiro indicated thatmosquito vectors (e.g., Ochlerotatus scapularis andOchlerotatus taeniorhynchus) are more abundant duringsummer months, but may also be captured in high num-ber in winter months [174]. These findings suggest thatdogs and cats may be at risk of D. immitis infestationduring the whole year, especially because the averageannual temperature in most of the Brazilian territory isbetween 21 and 30°C, which indeed facilitates the devel-opment of infective larvae (L3) in the mosquito vector.The presence of ectoparasites during the whole year

in Brazil is apparently the rule, not the exception.Phlebotomine sand fly vectors of Leishmania parasites

Figure 4 Vector density. Hundreds of phlebotomine sand flies (LutzomyiaPassira, north-eastern Brazil, where visceral leishmaniosis is endemic. (B) sh

such as L. longipalpis (Figure 4) and L. whitmani maybe found in high numbers throughout the year in differentBrazilian regions [175-180], even if some species maydisplay population peaks during the months of highestrainfall [181]. The same applies for fleas and ticks. Arecent study developed in south-eastern Brazil revealedhigh prevalence rates of flea (C. felis felis) and tick (A.cajennense and R. sanguineus s.l.) infestations during thedry and rainy seasons [35]. Another study carried out inthe same region indicated that R. sanguineus s.l. may infestdogs during any period of the year and completes threegenerations per year [182]. Similarly, an investigation con-ducted in centre-western Brazil suggested that this tickmay complete up to four generations per year [183].Again, these findings suggest that different Brazilian re-gions possess climate types and environmental conditionsthat enable the occurrence of ticks during all months ofthe year. For example, even if a study has identified varia-tions in B. vogeli infection in dogs apparently associatedwith peaks in the tick vector population [184], evidenceindicates that this protozoan may infect dogs at any periodof the year in some regions, regardless of the season [120].On the other hand, myiasis by C. hominivorax in dogs andcats presents a clearly defined seasonal pattern in Brazil,peaking during the hottest months of the year [59-61,65].Data concerning the seasonal dynamics of endopara-

sites in dogs and cats in Brazil is meagre. The incidenceof hookworm-related cutaneous larva migrans is higherduring the rainy season [185]. Interestingly, a studyreported a marked peak in Ancylostoma eggs sheddingin dog faeces during summer and autumn, suggestingthat winter conditions in São Paulo (south-eastern Brazil)have a negative effect on hookworm transmission [74].Another study concluded that the southern region ofBrazil has favourable edaphic and climatic conditionsfor soil contaminants (e.g., Toxocara eggs) to persist year-round, even if the species diversity of parasites was lowerin winter and the number of parasites lower in summer[186]. This is in agreement with studies carried out inother parts of South America. For instance, a study con-ducted in Mar del Plata, Argentina, reported a high

longipalpis) on a chicken (A) that was resting on a tree trunk inows a close-up of the phlebotomine sand flies


prevalence of intestinal parasites of dogs throughout theyear, with some seasonal variations according to the genusor species of parasite [187]. Hookworms (Ancylostomaspp.) were more prevalent in the summer-autumn period,ascarids (T. canis) in winter, whereas whipworms (T.vulpis) peaked in winter, spring and summer. Onceagain, these data demonstrate a high risk of parasiteinfestation in all seasons in this part of the Americas.

Diagnostic and management approachesDiagnosis of parasitic diseasesThe diagnosis of parasitic diseases affecting dogs andcats in Brazil is still predominately made by traditionalmethods. For instance, gastrointestinal parasites areusually detected by ordinary coprological techniques,such as Willis (flotation in saturated sodium chloridesolution), Faust (zinc sulphate centrifugal flotation) andHoffman-Pons-Janer (spontaneous faecal sedimentationin water) techniques [188,189]. These methods maypresent low sensitivity in some instances and result inthe underestimation of the real prevalence of some para-sites, such as D. caninum [74,77,100,188,190], when com-pared with necropsy data e.g., [32]. A commercial assayfor faecal concentration (namely, TF-test®) designed fordetecting human intestinal parasites [191] has also beenused for detecting helminth eggs, protozoan cysts andoocysts in canine faeces [190]. A comparative study re-vealed that the centrifugal flotation technique was moresensitive than centrifugal sedimentation and TF-test® indetecting Ancylostoma spp.,T. canis,T. vulpis and Giardiain dog faeces [190]. Another study reported that theWillis technique was more efficient in detecting eggs ofA. caninum and T. canis in dog faeces [188]. As a cor-ollary, a more recent study showed that the Willis andthe centrifugal flotation techniques performed betterthan the Hoffman-Pons-Janer technique for detectingAncylostoma spp. in dog faeces [189]. Other methodshave also been proposed, but apparently with no signifi-cant difference in terms of sensitivity, as compared withtraditional methods [98]. The use of an enzyme linked im-munosorbent assay (ELISA) for the detection E. granulo-sus coproantigen revealed high positivity rates (from 27.69to 47.37%) in rural dogs from southern Brazil [192]. In thesame way, PCR-based techniques have been used to detectendoparasites (heminths and protozoa) of dogs in Brazil e.g., [83,126,193,194] but currently these methods aremostly restricted to research.Blood-dwelling protozoan parasites (e.g., B. vogeli and

H. canis) are usually diagnosed by examination of stained-blood smears under a light microscope, which may lack insensitivity, particularly if blood samples are collected out-side the acute phase of the infection [195]. Serologicaltests are widely used to assess exposure to pathogens, suchas B. vogeli, Leishmania spp., N. caninum, and T. gondii

[168,169,184,196-198]. The use of molecular tools fordiagnosing protozoan parasites (e.g., B. vogeli, H. canis,and L. infantum) is becoming more and more popular, butit is still mostly restricted to research [121,199-204].Indeed, current PCR protocols have shown a good levelof concordance with parasitological methods [150].Unfortunately, the costs of molecular tools are stillprohibitive for most pet owners living in endemic areasand this severely impairs the diagnosis of diseases suchas visceral and cutaneous leishmaniosis in dogs. In-deed, current serological tools cannot distinguish betweenL. braziliensis and L. infantum [113,205]. This may havedirect implications for veterinary practitioners in Brazilbecause seropositive dogs are usually eliminated as part ofthe control programme against human visceral leishma-niosis, whilst it has been demonstrated that many of thesedogs are infected by L. braziliensis rather than L. infantum[113,205,206]. Indeed, the high diversity of parasites inBrazil may be a confounding factor for the diagnosis ofsome diseases in dogs and cats in this country. For in-stance, different Leishmania species have been reportedin these animals in Brazil and the clinical picture is notalways predictable. A recent report described a case ofcanine leishmaniosis by L. infantum in which the dogpresented a skin ulcer that is typically found in dogsand humans infected by L. braziliensis [207]. Again,dogs infected by L. amazonensis generally display clin-ical signs commonly observed in dogs with visceralleishmaniosis [96,117]. On the other hand, cats infectedby L. amazonensis typically display a cutaneous diseasethat resembles sporotrichosis [141,208]. It means thatthe same parasite may eventually induce different clin-ical diseases in dogs and cats, which emphasizes theneed for a proper laboratory diagnosis to confirm theparasite species involved. This is also true for eggs ofascarids (Toxocara spp.), and taenids (Taenia spp. andEchinococcus spp.) found in dog faeces, which cannot benormally differentiated by light microscopy [209,210].Hookworm eggs are not easily distinguishable bymorphology, but morphometric data suggests that theycan be differentiated [211]. Nonetheless, the use of im-proved, specific diagnostic techniques is fundamentaltowards a better management of parasitic diseases ofdogs and cats in Brazil.

Controlling dog and cat parasitesVeterinary practitioners working in Brazil are providedwith a relatively vast repertory of tools to control parasitesaffecting dogs and cats. Nonetheless, the control of com-mon parasites such as fleas and ticks may sometimes ap-pear quite difficult, mainly when the available tools arenot properly used or when veterinary practitioners do notpossess basic knowledge on the bio-ecology of some ofthese parasites. In Brazil, there are no official guidelines


for the control of ecto- and endoparasites of dogs andcats, such as those provided by European ScientificCounsel Companion Animal Parasites (ESCCAP: http://www.esccap.org/) in Europe and the Companion AnimalParasite Council (CAPC: http://www.capcvet.org/) in theUnited States. These guidelines are fundamental to ensurethe delivery of the latest scientific information on parasitecontrol to veterinary practitioners.Because lice and mites live in permanent association

with their hosts, they are relatively easily controlled and,once eliminated, re-infestation only occurs following con-tact with other infested animals [212,213]. As such, thecontrol of louse infestations in dogs and cats is mostlybased on the application of insecticides on infested ani-mals, which may be available as collars, spot-on solutions,and sprays [214-216]. Mites are also permanent ectopara-sites, with some of them living in the fur (L. radovskyi),others in the outer ear canal (O. cynotis), hair folliclesand sebaceous glands (D. canis and D. cati), or even ingalleries burrowed under the epidermis (N. cati e and S.scabiei). The treatment may be systemic (e.g., oral selamec-tin for S. scabiei) or topic (e.g., amitraz dip for D. canis).For instance, the treatment of infestations by the catfur mite (L. radovskyi) in Brazil has been successfullyperformed with weekly baths using a soap containingtetramethylthiuram monosulfide [217]. Similarly, a singlesubcutaneous injection of doramectin 1% (0.3 mg/kg) hasbeen effective in treating dogs with sarcoptic mange andendoparasites as well [218]. However, the treatment ofdemodicosis in dogs may vary depending on case severity,animal age, and the presence of underlying conditions[219]. Indeed, most young dogs with juvenile-onset local-ized demodicosis will resolve spontaneously without treat-ment, whereas adult dogs with generalized demodicosisusually require aggressive therapy, for example, with ami-traz dip every two weeks for several months [219]. Fur-thermore, an underlying disease or condition (e.g., cancer,hyperadrenocorticism, use of immunosuppressive drugs)should always be investigated and treated accordingly,especially in cases of demodicosis in adult dogs. It isclear that the treatment of mange in dogs and cats de-pends on several factors linked to the mite species in-volved and to the characteristics of each individualpatient. Veterinary practitioners should use the prod-ucts specifically labelled for mange treatment in dogsand cats in Brazil and strictly follow the manufacturer’srecommendations.In contrast to mites and lice, ticks and fleas are non-

permanent parasites [212] and therefore specimensfound on dogs and cats may represent only a small pro-portion of the whole flea and tick population present inthe environment where infested animals live. A vast rep-ertory of products are available in the veterinary marketin Brazil for controlling fleas and ticks on dogs and cats.

Insecticides and acaricides with potent anti-feeding andfast killing effects, repellents, insect growth regulators,and juvenile hormone analogues are available as spot-onpipettes, collars, shampoos, and sprays [212,220]. However,before deciding the best control strategy to be adopted, theveterinary practitioner should also investigate the presenceand the abundance of fleas/ticks in the environment wherethe animal lives. Ticks tend to drop off during the nightwhen the dog is sleeping [221]. Moreover, flea eggs are notsticky, falling from the animal’s fur in the environmentalong with adult flea faeces. Newly hatched larvae usuallyavoid sunlight and actively move deep into carpet fibres orunder organic debris [222]. Vacuuming places frequentedby pets (e.g., carpets, furniture cushions, rugs, or othersubstrata), with a vacuum cleaner as well as washing ofpet bedding or bed linen frequented by pets will help inthe removal of flea eggs and larvae [222]. Furthermore,the treatment of the indoor and outdoor environmentwith insecticides and acaricides may be required in somesituations, such as in kennels and catteries with high levelsof environment flea and tick infestation. Care should betaken when applying chemical products in the environ-ment and it is advisable that pet owners consult with a vet-erinarian or licensed pest control specialist [222].The chemical control of other arthropods (e.g., kissing

bugs, mosquitoes, and phlebotomine sand flies) in theenvironment is more complex and should also be per-formed in conjunction with public health authorities.For example, because mosquito larvae and pupae arestrictly associated with water collections (e.g., containers,deactivated swimming pools, abandoned tyres), theirpopulation may be reduced and sometimes eradicatedlocally by destroying their breeding sites or by using bio-logical control agents, such as the Bacillus thuringiensisisraelensis and fishes such as bettas (Betta splendens) andguppies (Poecilia reticulata) [223,224]. The spraying ofhouses and animal shelters (e.g., chicken pen) with re-sidual insecticides has long been recommended for con-trolling insect vectors, such as phlebotomine sand flies inBrazil [225,226]. However, results indicate that an effectivevector population control may be difficult to achieve andresistance to insecticides currently in use in Brazil hasbeen documented [227,228]. The use of insecticide-treatedbed nets has also been proven to be effective in protectinghumans against L. longipalpis bites [229], but this strategyis not currently used in Brazil as part of the nationalprogramme against zoonotic visceral leishmaniosis.The control of common endoparasites of dogs (e.g., A.

caninum and T. canis) and cats (e.g., A. braziliense andT. cati) usually consists of the routine administration ofanthelminthics associated with vector control for thosethat are vector borne (e.g., D. caninum, D. immitis, andP. praeputialis); reviewed in Ref. [8]. Indeed, the controlof zoonotic tapeworms (e.g., E. granulosus) may be

http://www.esccap.org/

http://www.esccap.org/

http://www.capcvet.org/


effectively performed by the systematic use of prazi-quantel. For instance, a pilot control programme was con-ducted in southern Brazil, in which 44 rural dogs weretreated monthly with praziquantel during 8 months [192].At the beginning of the programme, 17 out 44 (28%) dogswere positive for E. granulosus coproantigens by ELISAand 30 days after the last treatment administration no dogwas found positive [192]. Specifically, in the case of thedouble-pore tapeworm D. caninum, the control of fleasand lice is also advocated [8].The level of awareness and compliance of pet owners

may be low in some settings, particularly in outskirtsand rural areas. Even if an important part of pet ownersin Brazil cannot handle the costs of year-round prevent-ive programmes, the lack of compliance of wealthypeople to cope with veterinary recommendations is usu-ally due to their reduced risk perception. Alternativestrategies have been proposed, including the use of thenematophagous fungus Pochonia chlamydosporia as abiological control agent against embryonated eggs of T.canis [230]. Nevertheless, these alternatives are still a bit farfrom reality in Brazil.Finally, the control of vector-borne parasites is usually

based on the use of repellents on animals and on thecontrol of arthropod vectors in the environment, when-ever applicable [9,231]; e.g., for the control of H. canis,which is associated with high levels of environmentaltick infestation [232,233]. However, other strategies suchas dog culling have long been used in Brazil to controlzoonotic visceral leishmaniasis, even if this strategy hasbeen considered unethical and scientifically unsound [234].Recently, the Minister Joaquim Barbosa, President ofthe Supreme Federal Court of Brazil, refused the requestto suspend the judgment of the Interministerial Ordin-ance 1.426/2008, which prohibits the treatment and rec-ommends the euthanasia of L. infantum-infected dogs(www.brasileish.com.br/dados/artigos/artigos38155712122013.pdf). The Minister stated that this Ordinance violates theFederal Constitution and that the public power shouldfind alternatives to confront this issue, in partnership withscientists and veterinarians.

Prevention is better than cureMost dog owners seek the aid of a veterinary practitioneronly when their animals display overt disease signs. This isparticularly true in developing countries, where most dogowners cannot handle the costs of year-round preventiveprogrammes. Naturally, in some rural and suburban areasthe level of compliance may be even more reduced. None-theless, a considerable number of pet owners are increas-ingly aware of the risks and potential costs attached to thenon-adoption of preventive measures directed at avoidingthe exposure to certain pathogens, such as L. infantum.Thus, it is fundamental that veterinary practitioners

recommend preventatives to pet owners towards the es-tablishment of a long-term preventive programme againstendoparasites and ectoparasites in Brazil.The only vaccines against parasitic diseases available in

Brazil are those against leishmaniosis, which are designedand approved against “canine leishmaniosis”, not against“L. infantum infection”. Indeed, none of the currentlyavailable vaccines against canine leishmaniosis will preventdogs from becoming infected by L. infantum, but theyshould reduce the probability of vaccinated dogs to de-velop overt disease [231]. Importantly, if a vaccinateddog is able to mount an effective immune responseagainst L. infantum, it will probably maintain the para-sitic burden at low levels, eventually representing a poorsource of parasites to phlebotomine vectors [235]. Butagain, it is important to emphasize that vaccines are notrepellents and thus will not prevent dogs from beingbitten by phlebotomine sand flies [235].The use of repellents on dogs is an important strategy

against ectoparasites and the pathogens they transmit[236-238]. Currently, there are several products formu-lated as spot-on solutions, collars, and sprays with fast kill-ing effects, but synthetic pyrethroids remain the onlychemical compounds with repellent properties available inthe global veterinary market [239]. By virtue of theirrepellent and anti-feeding effects, synthetic pyrethroids(e.g., deltamethrin and permethrin) are highly efficaciousagainst ectoparasites such as fleas, lice, sand flies, andticks, but may also help to prevent the transmission ofpathogens such as B. vogeli, E. canis, and L. infantum[236-238]. In the same way, some products with a fast kill-ing effect are able to interrupt the attachment and bloodfeeding processes at their very early stages, thus also redu-cing the risk of pathogen transmission [240,241].

Dogs, cats, parasites and humans: public health aspectsWhile some dog and cat ectoparasites are strictly associatedto these animals, some of them may also infest humans.For instance, cases of human infestation by dog-associatedticks (e.g., A. aureolatum, A. ovale, and R. sanguineus s.l.)have sporadically been described in different Brazilian re-gions [242-247]. Cases of human infestations by dog ticks(R. sanguineus s.l.) appear to be associated with high levelsof environmental infestation in human dwellings and withpeople working in veterinary clinics or kennels [242,244].Importantly, some of these ticks may potentially transmitlife-threatening pathogens to humans, including Rickettsiarickettsii [248]. For instance, R. sanguineus s.l. tickshave been implicated in the transmission of rickettsialorganisms (e.g., Rickettsia conorii, Rickettsia massiliae,and R. rickettsii) to humans in the Mexico, the UnitedStates and the Mediterranean region [3]. Moreover, casesof human ehrlichiosis by E. canis have been described inVenezuela [249] and there is serological evidence that

http://www.brasileish.com.br/dados/artigos/artigos38155712122013.pdf

http://www.brasileish.com.br/dados/artigos/artigos38155712122013.pdf

Figure 5 Environmental contamination with dog faeces. Straydogs roaming freely in a beach in southern Brazil. Dog faeces are animportant source of zoonotic parasites that may cause diseases suchas cutaneous larva migrans.


humans may be in jeopardy of being infected by E. canisin Brazil as well [250]. Importantly, E. canis is widespreadand highly prevalent in Brazil [199,251-255], being pri-marily vectored by R. sanguineus s.l. ticks [256]. Casesof human infestation by Ctenocephalides spp. fleas havealso been reported in Brazil [13,257], and it is nowacknowledged that those fleas may carry Rickettsia felis[258], an emerging human pathogen worldwide [259]. Itmeans that the control of some common dog and catectoparasites (e.g., C. felis felis and R. sanguineus s.l.) isfundamental not only for their health, but also to safe-guard the health of their owners.Ascarids (Toxocara spp.) and hookworms (Ancylos-

toma spp.) of dogs and cats are parasites of great veter-inary and public health relevance, even if the generalperception of pet owners is that intestinal parasites of dogsand cats are of minor public health significance; reviewedin Ref. [260]. For instance, a study carried out in south-eastern Brazil revealed that most dog owners do notknow the species of dog intestinal parasites, the mecha-nisms of transmission, the risk factors for zoonoticinfections, and specific prophylactic measures [100]. None-theless, a number of cases of visceral and cutaneous larvamigrans in humans have been described in Brazil [261-264]and serological data confirmed a high level of exposureto Toxocara spp. in humans in this country, reachingover 50% in some cities [265-269]. Accordingly, highlevels of environmental contamination by Toxocara andAncylostoma eggs in public parks and squares have beenreported in different Brazilian regions [270-274]. Further-more, human lagochilascariasis is an emerging zoonosis inthe Americas caused by the roundworm Lagochilascarisminor and has been sporadically reported in Brazil[275-279], which holds the largest number of humancases reported in the literature [280]. Cats have beenfound naturally infested by L. minor and Lagochilascarismajor in Brazil [281-283]. Indeed, the role of cats asreservoirs of L. minor has been speculated [284] and thecontamination by Lagochilascaris eggs in public play-grounds has been documented in southern Brazil [285].The soil contamination by dog and cat faeces is a commonphenomenon in public gardens, sand boxes, and beaches(Figure 5) in Brazil, not only due to the large population ofstray animals present in the cities, but also due to the lackof proper sanitary and health education of some petowners.Tapeworms are also an underestimated problem in

Brazil and other South American countries. For instance,human cases of D. caninum have been described in Brazil[286-288]. Indeed, the high prevalence of D. caninum indogs in Brazil (e.g., 45.7% in north-eastern and 36.8% insouth-eastern Brazil) [32,36] is a consequence of the highprevalence of flea and lice infestations reported in differentregions of the country [18,28,30,32,35] and indicates a

high risk of zoonotic transmission in humans, particu-larly children, who live in close contact with infectedanimals. In the same way, cystic echinococcosis causedby E. granulosus is one of the most prevalent zoonosisin Argentina, Brazil, Chile, Peru, and Uruguay [289],being highly prevalent in southern Brazil, where up to50% of the dogs may be infested [72,290]. While othercanids (Pseudalopex gymnocercus, Cerdocyon thous,and Chrysocyon brachyurus) have been found naturallyinfested by E. granulosus in southern Brazil [290], dogsare the main reservoir of the parasite. In southern Brazil,E. granulosus is maintained principally in a dog-sheepcycle, with the sheep strain (G1) as the most prevalentgenotype; reviewed in Ref. [290]. Furthermore, humancases of polycystic echinococcosis by Echinococcus vogelihave been diagnosed in northern Brazil [291] and dogshave also been suspected to play a role in the zoonotictransmission of this parasite in the Neotropical region[292]. Similarly, experimental evidence indicates that catsmay act as definitive hosts for E. oligarthrus [293], anotheragent of polycystic echinococcosis in humans in LatinAmerica [292], which is traditionally associated with wildfelids. Last but not least, there is limited published infor-mation on other dog-associated taenids (e.g.,T. hydatigenaand T. multiceps) in Brazil [91], which suggests thathuman cysticercosis and coenuruses may be a silent,underestimated public health problem in some regionsof this country.Human pulmonary dirofilariosis is another common, yet

underestimated public health issue in Brazil; reviewed inRef. [294]. Even if several human cases have been de-scribed in the literature, most cases are accidentally foundby chance on chest radiographies and chest computerizedtomography scans, which are usually requested for otherreasons [295]. Furthermore, even if most patients with


pulmonary dirofilariosis present no apparent clinical signs,many of them will present cough, chest pain, haemoptysis,and dyspnoea [295-298]. Most importantly, the presenceof pulmonary nodules could lead to the suspicion of dis-eases such as tuberculosis or lung cancer and in thesecases thoracotomy is usually recommended. Indeed, hu-man pulmonary dirofilariosis is a public health issue thathas been so far neglected in Brazil. In the same way, therecent report of a case of ocular dirofilariosis in northernBrazil [299] suggests the risk of Dirofilaria infestation incertain Brazilian regions may be higher than currentlyappreciated.Zoonotic protozoa are also a serious public health issue

in Brazil. For instance, thousands of human cases of vis-ceral leishmaniosis caused by L. infantum are notified eachyear to the Ministry of Health, but control measuresmostly based on the elimination of seropositive dogs, vec-tor control (in specific situations) and human treatmenthave not been enough to control the disease [300]. Indeed,human visceral leishmaniosis is widespread in all Brazilianregions, being less common in the southern part ofthe country [301]. The occurrence of asymptomaticLeishmania infections in humans has been documentedin different regions of the country [302-304] and even ifthe Ministry of Health of Brazil affords the treatment ofhuman patients, the lethality rate may reach 18.4% ormuch higher in some settings [305-307]. Another import-ant zoonotic protozoan is T. gondii, an opportunisticpathogen highly prevalent in Brazil. Indeed, studies indi-cate that up to 50% of elementary school children and50-80% of women of child-bearing age have anti-T.gondii antibodies; reviewed in Ref. [308]. A recent out-break of acute toxoplasmosis in an industrial plant in SãoPaulo, south-eastern Brazil, indicated that ingestion ofgreen vegetables (not meat or water) was associated withthe incidence of acute disease [309]. Another recent studyrevealed a high seropositivity (80%) among HIV-positivepatients from southern Brazil, some of which had a historyof neurotoxoplasmosis (4.8%) and ocular toxoplasmosis(1.6%) [310].Chagas disease caused by T. cruzi remains an im-

portant public health issue in the Americas, affectingabout 10% of the poorest people in the region [311].Dogs and cats are considered important reservoirs ofT. cruzi in the domestic cycle of transmission [312].For instance, studies indicate that around 15-50% ofdogs living in areas where Chagas disease is endemicare seropositive [313-318]. However, the real roleplayed by dogs and cats in the transmission cycle ofT. cruzi in the current epidemiological context ofChagas disease in Brazil is arguable, because the greatmajority of recent human cases have been associatedwith oral transmission, via the ingestion of contami-nated juices [319].

Final considerations and future research directionsBrazil holds a vast territory and one of the largest dogand cat populations on the Planet. The economic growthand the increasing level of human development recordedin Brazil are provoking profound changes in the attitudeof some dog owners and veterinary practitioners towardshigh-standard healthcare services. Nonetheless, the macro-economic boom masks historical inequalities in terms ofaccess to basic sanitation, decent housing, safe drinkingwater, health care and education at both local and regionallevels. So, in reality, many dog owners cannot afford pre-ventive measures and will act only when a life-threateningproblem is affecting their animals. Furthermore, Brazil isstill home to a large population of dogs and cats living as“strays” or “community” animals, not only in rural areas,but also in suburbs and large urban centres. Public healthauthorities are not able to manage these animals due tothe lack of adequate infrastructure and trained personnelto conduct an effective long-term population control pro-gram. As a result, pet dogs and cats are usually endan-gered by a wide range of parasites that may cause diseasein them and eventually in their human counterpart.This invariably brings us to the One Health concept,which invites veterinary practitioners and medical phy-sicians to unify their efforts to combat zoonotic para-sites (e.g., T. canis, A. caninum, D. caninum, D. immitis,E. granulosus, and L. infantum). Indeed, the unificationof “veterinary and human medicines” in One Medicineis fundamental, instrumentally to reduce health hazardsto pet animals and humans.The outstanding diversity of ectoparasites infesting

dogs and cats in Brazil is certainly a consequence of acombination of factors. The variety of natural environ-ments and climates occurring in this country is impres-sive and favours the establishment of different parasitesin all geographical regions. In the same way, dogs andcats living in either urban or rural areas may eventuallylive in close contact with livestock and wildlife species(e.g., foxes, wild cats, and opossums), which ultimatelymay favour the exchange of ectoparasites such as fleasand ticks with these animals [320-323]. For instance, R.sanguineus s.l. has been found on coati (Nasua nasua)living in a zoological park in a large urban area innorth-eastern Brazil [322]. Even if this is an accidentalfinding, it suggests the presence of stray dogs circulat-ing freely within the park’s territory and living in closecontact with captive wild animals. Conversely, dogs andcats intruding or living near to forested environmentsmay be found infested by wildlife-associated ectoparasites[12,28,50,321]. The exchange of ectoparasites between do-mestic and wild animals may also have implications froma conservational perspective, also because dogs mayexchange endoparasites [324-326] and viruses [327,328]with wildlife species. For example, several wild canids


(e.g., C. thous and P. gymnocercus) and felids (e.g., Pantheraonca, Puma concolor, Puma yagouaroundi, and Leoparduspardalis) have been found harbouring parasites that mayaffect dogs and cats, including heminths (e.g., A. caninum,D. caninum, T. canis, and T. vulpis) and protozoa (e.g.,L. infantum) [324-326,329-333]. Remarkably, while free-roaming wild canids infected with L. infantum are usu-ally asymptomatic, captive ones seems to be more proneto develop clinical signs [329] and may even die frominfection [332].Veterinary practitioners working in Brazil are provided

with a vast repertory of products with proven efficacyagainst dog and cat parasites. Indeed, the registration ofveterinary products in Brazil involves several phases andstrict regulatory requirements [334]. However, the successof any parasite control programme depends on the correctuse of the chosen product(s) and on the adoption of thebest strategy for each situation. As previously discussed,guidelines for the diagnosis, treatment and control of dogand cat parasites in Brazil are currently lacking and are ur-gently needed. In the meantime, veterinary practitionersworking in Brazil should adhere strictly to manufacturers’instructions while using commercially available productsand follow international guidelines for the control of dogand cat parasites, eventually adapting them to regional sit-uations. In addition, the Brazilian Ministry of Agriculture,Livestock and Food Supply recently established the useof a passport for international transit of dogs and cats(http://www.estadao.com.br/noticias/geral,caes-e-gatos-terao-passaporte-e-identificacao-eletronica,1099476,0.htm).This passport will be used as a health certification oforigin and will include information about ecto- andendoparasite control. This will help to reduce the risk ofunintentional exportation of parasites from Brazil tooverseas.There are many outstanding questions regarding para-

sites of dogs and cats in Brazil, some of which may havealready been answered at the time that this manuscriptis being drafted. For instance, it is important to under-stand why some parasites are apparently restricted tothe southern and south-eastern regions of Brazil [9].This is the case of R. vitalii and B. gibsoni, for example.While B. gibsoni is a relatively rare parasite in dogs inBrazil, R. vitalii is quite common in southern and south-eastern states and may cause severe disease that can beeasily misdiagnosed with babesiosis or ehrlichiosis. Inter-estingly, the vectors of both protozoa remain unknown,but Amblyomma aureolatum is the putative vector forR. vitalii, at least. With this regard, the role of R. sangui-neus s.l. in the natural cycle of H. canis in Brazil needsfurther investigation. Accordingly, other tick specieshave been implicated as putative vectors of this orallytransmitted protozoan, including A. ovale [335,336] andRhipicephalus microplus [337]. Some parasites of dogs

and cats have only rarely been reported in Brazil, prob-ably due to the limited research effort on these littlestudied parasites, whose veterinary and medical signifi-cance has yet to be ascertained. For instance, enigmaticparasites such as Cercopithifilaria bainae [338] have beenoriginally described in Brazil, but remained doubtful andneglected for long time. Recently, this nematode was rede-scribed and it is emerging as a common filarioid of dogsin different European countries [339,340]. Altogether, theseexamples evidence that much has still to be discovered inBrazil regarding parasites of dogs and cats.Further research on dog and cat parasites in Brazil may

also reveal the existence of new species that have beenoverlooked over the years. Indeed, the use of molecularbiology is revolutionizing in a positive fashion our know-ledge on some “well-known” parasites, such as the browndog tick R. sanguineus s.l. [52,161,162,341]. Likewise,genetic data suggested that nematodes identified asA. vasorum in dogs from South America may representa different species from that observed in European dogs[342]. In this perspective, the use of molecular biologytechniques should become a reality in the daily routineof veterinary practitioners working in Brazil and there-fore the development of rapid, economically accessiblemolecular tools should be a research priority. For ex-ample, serological tests currently used by public author-ities are not able to discriminate dogs infected byL. infantum from those infected by L. braziliensis or evendistinguish vaccinated from naturally infected dogs [343].Therefore, veterinary practitioners should request add-itional tests (e.g., parasite isolation and characterization,PCR and DNA sequencing) to confirm whether the dog isactually infected by L. infantum in order to avoid the elim-ination of dogs infected by other parasites and to decideabout the most appropriate therapeutic approach to beadopted. With this respect, it is also important to monitorthe emergence of resistance to certain active principles(e.g., amitraz, fipronil, deltamethrin, and permethrin),as these compounds have long been used for ectopara-site control in Brazil. Likewise, there is no informationregarding the efficacy level of some endoparasiticides (e.g.,praziquantel, pyrantel, febantel, and ivermectin), which arewidely used in different Brazilian regions. These issuesshould be included in the research agenda of parasitolo-gists in Brazil in order to anticipate problems related toparasite resistance to active principles currently used forcontrolling ectoparasites and endoparasites of dogs andcats in this country.

ConclusionsIn conclusion, the benefits of having a dog or a cat as apet are undisputed, but the limit between benefit andprejudice is subtle. Indeed, the close contact betweenpets and humans may involuntarily represent a hazard

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for humans. Therefore, to avoid the potential risks associ-ated to owning a pet dog or cat, it is fundamental to main-tain them in good health and protected from zoonoticpathogens. Beyond the shadow of a doubt, it is our job asveterinarians to ensure that pets and their owners may livein harmony without representing a menace to each other.But from a holistic perspective, veterinary practitionersand medical physicians should work together towards im-proving the wellbeing and general health of both animalsand humans. Paraphrasing a famous American singer, aOne Health approach could help us to “heal the world”and “make it a better place” for dogs, cats, and humans.

Additional file

Additional file 1: Portuguese version of this review article.

Competing interestsThe authors declare that they have no competing interests.

Authors’ contributionsFD-T wrote the manuscript and DO reviewed it critically. Both authorsapproved the final version of the manuscript.

AcknowledgementsNovartis Animal Health supported the preparation of this review. Thanks toVinícius Roratto (Figure 1), Thiago André S. de Andrade (Figure 2), FernandoSilva and Pietra Lemos Costa (Figure 4), and Carlos A. P. Parchen (Figure 5)for sharing their photos. Thanks also to Viviana D. Tarallo for preparing theline drawings used in Figure 3, which were adapted from textbooks (e.g., Ref.[13]) and from photos kindly provided by Prof. Marcelo de Campos Pereira(http://www.icb.usp.br/~marcelcp/Default.htm).

Received: 13 November 2013 Accepted: 21 December 2013Published: 14 January 2014

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doi:10.1186/1756-3305-7-22Cite this article as: Dantas-Torres and Otranto: Dogs, cats, parasites, andhumans in Brazil: opening the black box. Parasites & Vectors 2014 7:22.

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